A centriolar FOP-like protein required for paraflagellar rod assembly, but not axoneme assembly in African trypanosomes: Trypanosome FOPL function

Jane Harmer, Katie Towers, Max Addison, Sue Vaughan, Paul McKean, Michael Ginger

Research output: Contribution to journalArticle

Abstract

Proteins of the FGR1 oncogene partner (or FOP) family are found at microtubule organising centres (MTOCs) including, in flagellate eukaryotes, the centriole or flagellar basal body from which the axoneme extends. We report conservation of FOP family proteins, TbFOPL and TbOFD1, in the evolutionarily divergent sleeping sickness parasite Trypanosoma brucei, showing in contrast to mammalian cells where FOP is essential for flagellum assembly, depletion of a trypanosome FOP homologue, TbFOPL, affects neither axoneme nor flagellum elongation. Instead, TbFOPL depletion causes catastrophic failure in assembly of a lineage-specific, extra-axonemal structure, the paraflagellar rod (PFR). That depletion of centriolar TbFOPL causes failure in PFR assembly is surprising since PFR nucleation commences ~2 μm distal from the basal body. When over-expressed with a C-terminal myc-epitope, TbFOPL was also observed at mitotic spindle poles. Little is known about bi-polar spindle assembly during closed trypanosome mitosis, but indication of a possible additional MTOC function for TbFOPL parallels MTOC localisation of FOP-like protein TONNEAU1 in acentriolar plants. More generally, our functional analysis of TbFOPL emphasizes significant differences in evolutionary cell biology trajectories of FOP-family proteins. We discuss how at the molecular level FOP homologues may contribute to flagellum assembly and function in diverse flagellates.
LanguageEnglish
Number of pages13
JournalOpen Biology
DOIs
Publication statusPublished - 25 Jul 2018

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Microtubule-Organizing Center
Axoneme
Trypanosomiasis
Flagella
Basal Bodies
Spindle Poles
Centrioles
Trypanosoma brucei brucei
Spindle Apparatus
Proteins
Oncogene Proteins
Eukaryota
Mitosis
Cell Biology
Cytology
Epitopes
Parasites
Functional analysis
Elongation
Poles

Cite this

@article{922393bf2f5a4384b75c8299b015fce6,
title = "A centriolar FOP-like protein required for paraflagellar rod assembly, but not axoneme assembly in African trypanosomes: Trypanosome FOPL function",
abstract = "Proteins of the FGR1 oncogene partner (or FOP) family are found at microtubule organising centres (MTOCs) including, in flagellate eukaryotes, the centriole or flagellar basal body from which the axoneme extends. We report conservation of FOP family proteins, TbFOPL and TbOFD1, in the evolutionarily divergent sleeping sickness parasite Trypanosoma brucei, showing in contrast to mammalian cells where FOP is essential for flagellum assembly, depletion of a trypanosome FOP homologue, TbFOPL, affects neither axoneme nor flagellum elongation. Instead, TbFOPL depletion causes catastrophic failure in assembly of a lineage-specific, extra-axonemal structure, the paraflagellar rod (PFR). That depletion of centriolar TbFOPL causes failure in PFR assembly is surprising since PFR nucleation commences ~2 μm distal from the basal body. When over-expressed with a C-terminal myc-epitope, TbFOPL was also observed at mitotic spindle poles. Little is known about bi-polar spindle assembly during closed trypanosome mitosis, but indication of a possible additional MTOC function for TbFOPL parallels MTOC localisation of FOP-like protein TONNEAU1 in acentriolar plants. More generally, our functional analysis of TbFOPL emphasizes significant differences in evolutionary cell biology trajectories of FOP-family proteins. We discuss how at the molecular level FOP homologues may contribute to flagellum assembly and function in diverse flagellates.",
author = "Jane Harmer and Katie Towers and Max Addison and Sue Vaughan and Paul McKean and Michael Ginger",
year = "2018",
month = "7",
day = "25",
doi = "10.1098/rsob.170218",
language = "English",
journal = "Open Biology",
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publisher = "Royal Society Publishing",

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A centriolar FOP-like protein required for paraflagellar rod assembly, but not axoneme assembly in African trypanosomes : Trypanosome FOPL function. / Harmer, Jane; Towers, Katie; Addison, Max; Vaughan, Sue; McKean, Paul; Ginger, Michael.

In: Open Biology, 25.07.2018.

Research output: Contribution to journalArticle

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AU - Harmer,Jane

AU - Towers,Katie

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AU - McKean,Paul

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AB - Proteins of the FGR1 oncogene partner (or FOP) family are found at microtubule organising centres (MTOCs) including, in flagellate eukaryotes, the centriole or flagellar basal body from which the axoneme extends. We report conservation of FOP family proteins, TbFOPL and TbOFD1, in the evolutionarily divergent sleeping sickness parasite Trypanosoma brucei, showing in contrast to mammalian cells where FOP is essential for flagellum assembly, depletion of a trypanosome FOP homologue, TbFOPL, affects neither axoneme nor flagellum elongation. Instead, TbFOPL depletion causes catastrophic failure in assembly of a lineage-specific, extra-axonemal structure, the paraflagellar rod (PFR). That depletion of centriolar TbFOPL causes failure in PFR assembly is surprising since PFR nucleation commences ~2 μm distal from the basal body. When over-expressed with a C-terminal myc-epitope, TbFOPL was also observed at mitotic spindle poles. Little is known about bi-polar spindle assembly during closed trypanosome mitosis, but indication of a possible additional MTOC function for TbFOPL parallels MTOC localisation of FOP-like protein TONNEAU1 in acentriolar plants. More generally, our functional analysis of TbFOPL emphasizes significant differences in evolutionary cell biology trajectories of FOP-family proteins. We discuss how at the molecular level FOP homologues may contribute to flagellum assembly and function in diverse flagellates.

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